Analysis of DNA fragmentation, plasma membrane translocation of phosphatidylserine and oxidative stress in human spermatozoa

Human Reproduction

Volumn 15, Issue 6, 2000, Pages 1338-1344

  Barroso, Gerardo ^b   Morshedi, Mahmood ^b   Oehninger, Sergio ^a,b  

^a The Jones Institute for Reproductive Medicine   (United States)

^b EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

DNA fragmentation; Membrane phosphatidylserine; Reactive oxygen species; Spermatozoa

Indexed keywords

DNA; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE; SINGLE STRANDED DNA;

ARTICLE; CELL MEMBRANE; DNA DAMAGE; GENE TRANSLOCATION; HUMAN; MALE; MALE INFERTILITY; OXIDATIVE STRESS; SPERMATOZOON; SPERMATOZOON MOTILITY;

EID: 0034091122     PISSN: 02681161     EISSN: None     Source Type: Journal    
DOI: 10.1093/humrep/15.6.1338     Document Type: Article

References (76)

1. Aitken, R.J. and West, K.M. (1990) Analysis of the relationship between reactive oxygen species production and leukocyte infiltration in fractions of human semen separated on Percoll gradients. Int. J. Androl., 13, 433-451.
2. Aitken, R.J., Clarkson, J.S. and Fishel, S. (1989a) Generation of reactive oxygen species, lipid peroxidation and human sperm function. Biol. Reprod., 40, 183-197.
3. Aitken, R.J., Clarkson, J.S., Hargreave, T.B. et al. (1989b) Analysis of the relationship between defective sperm function and the generation of reactive oxygen species in cases of oligozoospermia. J. Androl., 10, 214-220.
4. Aitken, R.J., Irvine, D.S. and Wu, F.C. (1991) Prospective analysis of sperm-oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am. J. Obstet. Gynecol., 164, 542-551.
5. Aitken, R.J., Buckingham, D.W. and West, K.M. (1992) Reactive oxygen species and human spermatozoa: Analysis of the cellular mechanisms involved in luminol-and lucigenin-dependent chemiluminescence. J. Cell. Physiol., 151, 466-477.
6. Aitken, R.J., Gordon, E., Harkiss, D. et al. (1998) Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol. Reprod., 59, 1037-1046.
7. Alvarez, J.G., Touchstone, J.C., Blasco, L. et al. (1987) Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa. Superoxide dismutase as major enzyme protectant against oxygen toxicity. J. Androl., 8, 338-348.
8. Aravindan, G.R., Bjordahl, J., Jost, L.K. et al. (1997) Susceptibility of human sperm to in situ DNA denaturation is strongly correlated with DNA strand breaks identified by single-cell electrophoresis. Exp. Cell Res., 236, 231-237.
9. Ashkenas, J. and Werb, Z. (1996) Proteolysis and the biochemistry of life-or-death decisions. J. Exp. Med., 183, 1947-1951.
10. Baccetti, B., Collodel, G., Piomboni, P. (1996) Apoptosis in human ejaculated sperm cells (notulae seminologicae 9). J. Submicrosc. Cytol. Pathol., 28, 587-596.
11. Brunner, T., Mogil, R.J., LaFace, D. et al. (1995) Cell-autonomous Fas (CD95)/Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature (Lond.), 373, 441-444.
12. Burkman, L.J. (1991) Discrimination between nonhyperactivated and classical hyperactivated motility patterns in human spermatozoa using computerized analysis. Fertil. Steril., 55, 363-371.
13. Charriaut-Mariangue, C. and Ben-Ari, Y. (1995) A cautionary note on the use of the TUNEL stain to determine apoptosis. NeuroReport, 1, 61-64.
14. D'Cruz, O.J., Dong, Y., Uckun, F.M. (1999) Spermicidal activity of oxovanadium (IV) complexes of 1,10-phenanthroline, 2,2′-bipyridyl, 5′-bromo-2′-hydroxyacetophenone and derivatives in humans. Biol. Reprod., 60, 435-44
15. de Lamirande, E. and Gagnon, C. (1993a) A positive role for the superoxide anion in the triggering of human sperm hyperactivation and capacitation. Int. J. Androl., 16, 21-25.
16. de Lamirande, E. and Gagnon, C. (1993b) Human sperm hyperactivation as part of an oxidative process. Free Radical Biol. Med., 314, 157-166.
17. Desjardins, L.M. and MacManus, J.P. (1995) An adherent cell model to study different stages of apoptosis. Exp. Cell Res., 216, 380-387.
18. Dhein, J., Walczak, H., Bäumler, C. et al. (1995) Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature (Lond.), 373, 438-441.
19. Evenson, D.P., Darzynkiewicz, Z. and Melamed, M.R. (1980) Relation of mammalian sperm chromatin heterogeneity to fertility. Science, 240, 1131-1133.
20. Evenson, D.P., Jost. L.K., Marshall, D. et al. (1999) Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum. Reprod., 14, 1039-1049.
21. Fadok, V.A., Voelker, D.R., Campbell, P.A. et al. (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol., 48, 2207-2216.
22. Fraga, C.G., Motchnik, P.A., Wyrobek, A.J. et al. (1996) Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutat. Res., 351, 199-203.
23. Frankfurt, O.S. (1994) Detection of apoptosis in leukemic and breast cancer cells with monoclonal antibody to single-stranded DNA. Anticancer Res., 14, 1861-1870.
24. Frankfurt, O.S., Seckinger, D. and Sugarbaker, E.V. (1994) Apoptosis and growth inhibition in sensitive and resistant leukemic cells treated with anticancer drugs. Int. J. Oncol., 4, 481-489.
25. Frankfurt, O.S., Robb, J.A., Sugarbaker, E.V. et al. (1996) Monoclonal antibody to single-stranded DNA is a specific and sensitive cellular marker of apoptosis. Exp. Cell Res., 226, 387-397.
26. Frankfurt, O.S., Robb, J.A., Sugarbaker, E.V. et al. (1997) Apoptosis in breast carcinomas detected with monoclonal antibody to single-stranded DNA: Relation to bcl-2 expression, hormone receptors and lymph node metastases. Clin. Cancer Res., 3, 465-471.
27. Gavrieli, Y., Sherman, Y. and Ben-Sasson, A. (1991) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol., 119, 493-501.
28. Glander, H.-J. and Schaller, J. (1999) Binding of annexin V to plasma membranes of human spermatozoa: a rapid assay for detection of membrane changes after cryostorage. Mol. Hum. Reprod., 5, 109-115.
29. Gold, R., Schmied, M., Giegerich, G. et al. (1994) Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Lab. Invest., 71, 219.
30. Gorczyca, W., Traganos, F., Jesionowska, H. et al. (1993) Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: anology to apoptosis of somatic cells. Exp. Cell Res., 207, 202-205.
31. Grasl-Kraupp, B., Ruttkay-Nedecky, B., Koudelka, H. et al. (1995) In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology, 21, 1465-1468.
32. Hofmann, N. and Hilscher, B. (1991) Use of aniline blue to assess chromatin condensation in morphologically normal spermatozoa in normal and infertile men. Hum. Reprod., 6, 979-982.
33. Homburg, C.H.E., de Haas, M., von dem Borne, A.E.G.Kr. et al. (1995) Human neutrophils lose their surface FcγRIII and acquire Annexin V binding sites during apoptosis in vitro. Blood, 85, 532-540.
34. Hughes, C.M., Lewis, S.E.M., McKelvey-Martin, V.J. et al. (1996) A comparison of baseline and induced DNA damage in human spermatozoa from fertile and infertile men using a modified comet assay. Mol. Hum. Reprod., 2, 613-619.
35. Hughes, C.M., Lewis, S.E., McKelvey-Martin, V.J. et al. (1998) The effects of antioxidant supplementation during Percoll preparation on human sperm DNA integrity. Hum. Reprod., 13, 1240-1247.
36. Hughes, C.M., McKelvey-Martin, V.J. and Lewis, S.E. (1999) Human sperm DNA integrity assessed by the Comet and ELISA assays. Mutagenesis, 14, 71-75.
37. Iwasaki, A. and Gagnon, C. (1992) Formation of reactive oxygen species in spermatozoa of infertile patients. Fertil. Steril., 57, 409-416.
38. James, P.S., Wolfe, C.A., Mackie, A. et al. (1999) Lipid dynamics in the plasma membrane of fresh and cryopreserved human spermatozoa. Hum. Reprod., 14, 1827-1832.
39. Jarow, J.P. (1998) Detection of oxidative RNA damage in human sperm and the association with cigarette smoking. J. Urol., 159, 1774-1775.
40. Jones, R., Mann, T. and Sherins, R. (1979) Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertil. Steril., 31, 531-537.
41. Ju, S.-T., Panka, D.J., Cui, H. et al. (1995) Fas (CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature (Lond.), 373, 444-448.
42. Jurisicova, A., Lopes, S., Meriano, J. et al. (1999) DNA damage in round spermatids of mice with a targeted disruption of the Pp1cγ gene and in testicular biopsies of patients with non-obstructive azoospermia. Mol. Hum. Reprod., 5, 323-330.
43. Kerr, J. (1993) Definition of apoptosis and overview of its incidence. In Lavinand, M. and Watters, D. (eds), Programmed Cell Death. Harwood Academic Publishers, Langhorne, PA, USA, pp. 1-15.
44. Kodoma, H., Yamaguchi, R., Fukuda, J. et al. (1997) Increased oxidative deoxyribonucleic acid damage in the spermatozoa of infertile male patients. Fertil. Steril., 68, 519-524.
45. Krausz, C., West, K., Buckingham, D. and Aitken, R.J. (1992) Development of a technique for monitoring the contamination of human semen samples with leukocytes. Fertil. Steril., 57, 1317-1325.
46. Lee, B.R. and Um, H.-D. (1999) Hydrogen peroxide suppresses U937 cell death by two different mechanisms depending on its concentration. Exp. Cell Res., 248, 430-438.
47. Lin, W.W., Lamb, D.J., Wheeler, T.M. et al. (1997a) In situ end-labeling of human testicular tissue demonstrates increased apoptosis in conditions of abnormal spermatogenesis. Fertil. Steril., 68, 1065-1069.
48. Lin, W.W., Lamb, D.J., Wheeler, T.M. et al. (1997b) Apoptotic frequency is increased in spermatogenic maturation arrest and hypospermatogenic states. J. Urol., 158, 1791-1793.
49. Liu, D.Y. and Gordon Baker, H.W. (1992) Sperm nuclear chromatin normality: relationship with sperm morphology, sperm-zona pellucida binding and fertilization rates in vitro. Fertil. Steril., 58, 1178-1184.
50. Liu, D.Y. and Baker, H.W. (1994) Disordered acrosome reaction of spermatozoa bound to the zona pellucida: a newly discovered sperm defect causing infertility with reduced sperm-zona pellucida penetration and reduced fertilization in vitro. Hum. Reprod., 9, 1694-1700.
51. Lloyd, D.R., Phillips, D.H. and Carmichael, P.L. (1997) Generation of putative intrastrand cross-links and strand breaks in DNA by transition metal ion-mediated oxygen radical attack. Chem. Res. Toxicol., 10, 393-400.
52. Lopes, S., Jurisicova, A., Sun, J.-G. et al. (1998a) Reactive oxygen species: potential cause for DNA fragmentation in human spermatozoa. Hum. Reprod., 13, 896-900.
53. Lopes, S., Sun, J.-G., Jurisicova, A. et al. (1998b) Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil. Steril., 69, 528-532.
54. Manicardi, G.C., Bianchi, P.G., Pantano, S. et al. (1995) Underprotamination and nicking of DNA in ejaculated human spermatozoa are highly related phenomena. Biol. Reprod., 52, 864-867.
55. Manicardi, G.C., Tombacco, A., Bizzaro, D. et al. (1998) DNA strand breaks in ejaculated human spermatozoa: comparison of susceptibility to the nick translation and terminal transferase assays. Histochem. J., 30, 33-39.
56. Martin, S.J. and Green, D.R. (1995) Protease activation: Death by a thousand cuts? Cell, 82, 349-352.
57. Martin, S., Reutelingsperger, C., McGahon, A. et al. (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition of overexpression of Bcl-2 and Ab1. J. Exp. Med., 182, 1545-1556.
58. McPherson, S. and Longo, F. (1992) Localization of DNase I-hypersensitive regions during rat spermatogenesis: stage dependent patterns and unique sensitivity of elongating spermatids. Mol. Reprod. Dev., 31, 268-279.
59. Mortimer, D., Pandya, I.J. and Sawers, R.S. (1986) Relationship between human sperm motility characteristics and sperm penetration into human cervical mucus in vitro. J. Reprod. Fertil., 78, 93-102.
60. Nassar, A., Mahony, M., Blackmore, P. et al. (1998) Increase of intracellular calcium is not a cause of pentoxifylline-induced hyperactivated motility or acrosome reaction in human sperm. Fertil. Steril., 69, 748-754.
61. Oehninger, S., Blackmore, P., Mahony, M. et al. (1995) Effects of hydrogen peroxide on human spermatozoa. J. Assist. Reprod. Genet., 12, 41-47.
62. Oehninger, S., Lanzendorf, S., Burkman, L.J. et al. (1994) A sequential analysis of the effect of progesterone on specific sperm functions crucial to fertilization in-vitro in infertile patients. Hum. Reprod., 9, 1322-1327.
63. Oehninger, S., Mahony, M., Özgür, K. et al. (1997) Clinical significance of human sperm-zona pellucida binding. Fertil. Steril., 67, 1121-1127.
64. Oehninger, S., Toner, J.P., Muasher, S.J. et al. (1992) Prediction of fertilization in vitro with human gametes: is there a litmus test? Am. J. Obstet. Gynecol., 167, 1760-1767.
65. Sailer, B.L., Jost, L.K. and Evenson, D.P. (1995) Mammalian sperm DNA susceptibility to in situ denaturation associated with the presence of DNA strand breaks as measured by the terminal deoxynucleotidyl transferase assay. J. Androl., 16, 80-87.
66. Sakkas, D. (1999) DNA damage in human spermatozoa and the possible consequences on embryo development. Andrology in the Nineties, an International Symposium on Human Sub-fertility, Cape Town, South Africa, March 25-27, p. AL 37.
67. Sakkas, D., Mariethoz, E., Manicardi, G. et al. (1999) Origin of DNA damage in ejaculated human spermatozoa. Rev. Reprod., 4, 31-37.
68. Shen, H.M., Chia, S.E., Ni, Z. Y. et al. (1997) Detection of oxidative DNA damage in human sperm and the association with cigarette smoking. Reprod. Toxicol., 11, 675-680.
69. Sinha Hikim, A.P., Wang, C., Lue, Y. et al. (1998) Spontaneous germ cell apoptosis in humans: Evidence for ethnic differences in the susceptibility of germ cells to programmed cell death. J. Clin. Endocrinol. Metab., 83, 152-156.
70. Sun, J.-G., Jurisicova, A. and Casper, R.F. (1997) Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol. Reprod., 56, 602-607.
71. Tejada, R.I., Mitchell, J.C., Norman, A. et al. (1984) A test for the practical evaluation of male fertility by acridine orange (AO) fluorescence. Fertil. Steril, 42, 87-91.
72. Twigg, J., Fulton, N., Gomez, E. et al. (1998a) Analysis of the impact of intracellular reactive oxygen species generation on the structural and functional integrity of human spermatozoa: lipid peroxidation, DNA fragmentation and effectiveness of antioxidants. Hum. Reprod., 13, 1429-1436.
73. Twigg, J., Irvine, D.S., Houston, P. et al. (1998b) Iatrogenic DNA damage induced in human spermatozoa during sperm preparation: protective significance of seminal plasma. Mol. Hum. Reprod., 4, 439-445.
74. Van Blerkom, J. and Davis, P.W. (1998) DNA strand breaks and phosphatidylserine redistribution in newly ovulated and cultured mouse and human oocytes: occurrence and relationship to apoptosis. Hum. Reprod., 13, 1317-1324.
75. Verhoven, B., Schlegel, R.A. and Williamson, P. (1995) Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J. Exp. Med., 182, 1597-1601.
76. Vermes, I., Haanen, C., Steffens-Nakken, H. et al. (1995) A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods, 184, 39.